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J. Microbiol. Biotechnol. 2020. 30(7): 1013–1017 https://doi.org/10.4014/jmb.2001.01016

Endomicrobial Community Profiles of Two Different Mealybugs: Paracoccus

marginatus and Ferrisia virgata

Polpass Arul Jose1#, Ramasamy Krishnamoorthy1, Pandiyan Indira Gandhi2, Murugaiyan Senthilkumar3, Veeranan Janahiraman1, Karunandham Kumutha1,

  • 4
  • 4‡
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  • 4

  • *
  • *

Aritra Roy Choudhury , Sandipan Samaddar , Rangasamy Anandham , and Tongmin Sa

1Department of Agricultural Microbiology, Agricultural College and Research Institute, Madurai, Tamil Nadu Agricultural University, Tamil Nadu, India 2Regional Research Station, Vridhachalam, Tamil Nadu Agricultural University, Tamil Nadu, India 3Department of Agricultural Microbiology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India 4Department of Environmental and Biological Chemistry, Chungbuk National University, Cheongju 28644, Republic of Korea

Mealybugs (Hemiptera: Coccomorpha: Pseudococcidae) harbor diverse microbial symbionts that play essential roles in host physiology, ecology, and evolution. In this study we aimed to reveal microbial communities associated with two different mealybugs, papaya mealybug (Paracoccus marginatus) and two-tailed mealybug (Ferrisia virgata) collected from the same host plant. Comparative analysis of microbial communities associated with these mealybugs revealed differences that appear to stem from phylogenetic associations and different nutritional requirements. This first report on both bacterial and fungal communities associated with these mealybugs provides a preliminary insight on factors affecting the endomicrobial communities.

Received: January 13, 2020 Accepted: March 31, 2020

First published online: April 02, 2020

Keywords: Ecology, mealybug, endomicrobiota, phylogeny, Paracoccus marginatus Ferrisia virgata
,

*

Corresponding authors

T.S.

Insects are the most abundant animals in terrestrial ecosystems and are inhabited by symbiotic microbes that provide beneficial services to their hosts [1]. Mealybugs (Homoptera: Coccoidea: Pseudococcidae) are plantsucking scale insects affecting agricultural ecosystems and causing damage to more than 300 plant species [2-4]. Examining the ecological interactions of symbiotic microbes in agriculturally important insect-hosts may lead to novelmethods of pestcontrolandenhancementof agriculturalproductivity [5, 6]. Dietand theinsectlineagehave been proposed to exert different influences on symbiotic microbial diversity [7]. Accordingly, in this study we examined the hypothesis that the mealybug microbial ecology is strongly determined by interaction between phylogenetic constraints and nutritional requirements. To this end, we performed endomicrobial community analysis of two phylogenetically distinct mealybug species that feed concurrently on the same plant yet differ in their choice of feeding site and the processing of the plant-derived diet. 1) Papaya mealybug (PM), Paracoccus marginatus Williams and Granara de Willink, feeds frequently on phloem sap and produces large amounts of honeydew [8]. 2) Two-tailed mealybug (TM), Ferrisia virgata Cockerell, colonizes around the terminal parts of the plant, infrequently accesses the phloem sap and produces small amounts of honeydew [9]. Based on integrated molecular and morphological data, these two mealybugs have been assigned under different sub-families [10]. Pooled PM and TM samples were created from fifty individuals of each mealybug species collected from a papaya (Carica papaya) plant cv. CO8 at Agricultural College and Research Institute, Madurai (9°56'0" N and 78°7'0" E), India. The insects were surface sterilized by rinsing in sterile water, soaking in 70% ethanol and 10% bleach, with three rinses in water, for 60 sec at each step. The surface-sterilized insects were homogenized in liquid nitrogen. Whole DNA was extracted from homogenates using an Insect DNA Purification Kit (Hi-Media, India) according to the manufacturer’s protocol. The extracted DNA was amplified using primers targeting the V3-V4 region of the bacterial 16S rRNA gene (primers, 341F and 518R) and fungal internal transcribed spacer (primers, ITS5F and ITS2R) [11, 12]. Sequencing was performed using the Illumina MiSeq platform at Genotypic Technology, India. Resulted sequence data were deposited in SRA archives under accession number PRJNA522349. Theraw reads were processed as describedelsewhere[13]. Theprocessing ofrawreadsclustered at 97% identity revealed 5,881 and 2,417 bacterial operational taxonomic units (OTUs), whereas 258 and 172 fungal OTUs were identified for PM and TM, respectively. The rarefaction curve (Fig. S1) indicated the adequate sampling effort for getting the full extent of taxonomic diversity. It explains how the number of species found in a sampleat any given phylogenetic level is strongly affected by the number of sequences analyzed [14]. The Shannon

Phone: +82-43-261-2561 Fax: +82-43-271-5921 E-mail: [email protected] R.A. E-mail: anandhamranga@gmail. com

#Present address: Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, POB 12, Rehovot 761000, Israel ‡Present address: Department of Land, Air and Water Resources, University of California, Davis, California, USA

Supplementary data for this paper are available on-line only at http://jmb.or.kr.

pISSN 1017-7825 eISSN 1738-8872

Copyright 2020 by

©

The Korean Society for Microbiology and Biotechnology

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Table 1. Microbial diversity estimates in the gut of papaya mealybug and two-tailed mealybug.

  • Domain Type of mealybug Number of OTUs
  • Chao1 (Richness)
  • Shannon (Diversity) Simpson (Diversity)

Bacteria
PM

TM PM TM
5881 2417 258
10061.46 4833.76
276
3.42 1.87 1.30 0.54
0.64 0.48 0.91 0.48
Fungi

  • 170
  • 172

and Simpson diversity indices, and richness estimator (Chao) of bacteria and fungi were relatively higher for PM compared to TM (Table 1). However, the diversity and richness indices of fungi were relatively poor for both the samples compared to the bacterial counterpart. The gut bacterial community had proteobacterial abundance for both of the mealybug species, followed by Actinobacteria and Firmicutes in PM and TM, respectively (Fig. 1A). A previous study of 305 individual insects belonging to 21 taxonomic orders showed that the insect microbiota is dominated by the Proteobacteria and

Fig. 1. Bacterial community profile decoded by 16S amplicon-metagenomics. Relative abundance of the gut-

bacterial lineages (after removing endosymbionts) found in PM and TM at (A) phylum level and (B) species level.

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Firmicutes [15]. Moreover, the specific abundance of Proteobacteria further correlates well with bacterial communities of different mealybug species [16-18]. Recently, Iasur-Kruh et al. [17]reported that Betaproteobacteria (58%) and Gammaproteobacteria (33%) constituted the proteobacterial community in the vine mealybug. However, this pattern deviated in papaya and two-tailed mealybugs. In papaya mealybug, all the three classes of Proteobacteria (Betaproteobacteria (83.41%), Alphaproteobacteria (7.19%) and Gammaproteobacteria (4.63%) were represented, while Betaproteobacteria is most abundant (97.6%) in two-tailed mealybug (Fig. 1B). At the genus level, PM and TM samples were dominated by the obligate nutritional endosymbionts Tremblaya, which has been reported to provide aid in nutrition and detoxification of plant substances [19, 20]. The ITS sequencebased fungal community analysis revealed the occurrence of seven fungal phyla (Fig. 2A). The majority of sequences were affiliated with Ascomycota (78.75%), followed by Zygomycota (4.74%) and Basidomycota (5.91%). Individually, Ascomycota dominated with 75.28% and 91.65% in PM and TM respectively. The phylum Zygomycota and two different unclassified populations were moderately abundant in PM, while it was less abundant in TM. However, Glomeromycota was more abundant in TM rather than in PM. However, among the classified genera, Cladosporium showed moderate abundance (8.04%), followed by Aureobasidium (5.54%), Mortierella (4.61%). Notably, the majority of Aureobasidium and Mortierella counts were from PM (Fig. 2B). The results of earlier studies using culture-dependent and molecular techniques indicated that vine mealybug, Planococcus ficus, largely harbors Ascomycota [18]. Cladosporium and Mycosphaerella, common environmental fungi, were equally found in both TM and PM. Iasur-Kruh et al. [17] found that Cladosporium is abundant in vine mealybug reared in lab. This suggests that Cladosporium and Mycosphaerella are more transient fungal associates

Fig. 2. Fungal community profile decoded by 18S (ITS) amplicon-metagenomics. Relative abundance of the gut-

fungal lineages (after removing endosymbionts) found in PM and TM at (A) phylum level and (B) species level.

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Fig. 3. Functional mapping of the bacterial community associated with PM and TM.

acquired via feeding. A recent study using confocal microscopy revealed that a similar fungus, Beauveria bassiana, penetrates mealybug Phenacoccus manihoti through the legs and mouthparts [21]. Interestingly, several fungal species were found in one mealybug species, while not in the other, though they were sampled from the same plant. For instance, Zygomycota was found in PM, but not in TM. Similarly, Glomeromycota was found in TM, yet it is absent in PM. These differences could be due to selective ecological pressure exerted by the host [18, 22]. Among the symbionts associated with PM and TM, Tremblaya is a well-known endosymbiont of mealybugs. Bacterial communities other than Tremblaya associated with the PM and TM were retrieved from the taxonomy data and mapped for their metabolic activities using differentphenotypic categories in METAGENassist [23]. The analysis was done using the standard settings suggested in the server. The results revealed the occurrence of 15 types of metabolic activities (Fig. 3). Interestingly, abundant bacteria capable of ammonia oxidization, atrazine metabolism, dehalogenation, nitrate reduction, sulfur metabolism, and xylan degradation were found in both mealybug species. The automated metabolic functional mapping of the abundant bacterial community revealed diverse activities, and strongly suggested the role of the bacterial communities associated with both mealybugs in providing nutritional as well as detoxification support to the host insects. For instance, those microbes having the ability to fix and mobilize different nutrients (nitrogen and sulfur) could provide dietary support to the insect host, while others are involved in detoxification of toxic compounds [24]. Difference in the relative abundance of different metabolic functions suggests evolutionary trajectories of the microbial communities, tailored to specific needs of the hosts [24, 25]. Insummary, this study disclosed the endomicrobial communities (bacteria and fungi)intwo mealybug species, P. marg inatus and F. Virgata, differ in phylogenetic and nutritional characteristics. Despite a lack of sequencing replicates, this study provides a preliminary insight into the relationships between different mealybugs and their microbial communities. Differences among the microbial communities appear to be associated largely with their phylogeny and different nutritional characteristics while they fed on the same plant sap. The super dominant bacteria was Tremblaya in both cases, but intra generic diversity was found within this genus in PM. Dynamics of Tremblaya in PM, as well as the moderately abundant and rare species in both mealybug species have to be studied under controlled conditions to reveal their biological and symbiotic roles.

Availability of Data and Materials

The data and analyses from the current study are available from the corresponding author upon reasonable request. The raw reads were deposited in SRA archives and can be accessed by accession number PRJNA522349.

Acknowledgments

This study was supported by the Rapid Grant for Young Investigator (RGYI), Department of Biotechnology
(DBT), Ministry of Science and Technology, Government of India under grant no. BT/PR6430/GBD/27/412/ 2012. The authors are so grateful to Prof. Boaz Yuval for his critical reading of the manuscript.

Conflict of Interest

The authors have no financial conflicts of interest to declare.

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  • 4 Economic Value of Arthropod Biological Control

    4 Economic Value of Arthropod Biological Control

    ©CAB International – for Steven Naranjo 4 Economic Value of Arthropod Biological Control STEVEN E. NARANJO1*, GEORGE B. FRISVOLD2 AND PETER C. ELLSWORTH3 1USDA-ARS, Arid-Land Agricultural Research Center, Maricopa, AZ, USA; 2Department of Agricultural and Resource Economics, University of Arizona, Tucson, AZ, USA; 3Department of Entomology, University of Arizona, Maricopa Agricultural Center, Maricopa, AZ, USA Integrated pest management (IPM) is the strategic control are very low, successful programmes have integration of multiple control tactics resulting in the resulted in essentially permanent pest control with amelioration of pest damage that takes into consid- very favourable economic outcomes (Cock et al., eration environmental safety, and the reduction of 2015; Naranjo et al., 2015). risk and favourable economic outcomes for growers A second approach – augmentative biological and society at large. For thousands of years, natural control – involves the initial (inoculation) or enemies of pests have been harnessed for crop pro- repeated (inundation) introduction of native or tection (Simmonds et al., 1976). Maximizing this exotic natural enemies to suppress pest populations. source of natural control is a foundational element Augmentative biological control has been widely in IPM for suppressing the growth of incipient pest and successfully deployed in many parts of the populations (Stern et al., 1959). Biological control world. It is perhaps most well known in protected has been defined as the purposeful use of natural agricultural production, particularly in Europe and enemies, such as predators, parasitoids and patho- in developing regions such as China, India and gens, to regulate another organism’s populations to Latin America (van Lenteren et al., 2017).
  • Cryptolaemus Montrouzieri As a Predator of the Striped Mealybug, Ferrisia Virgata, Reared on Two Hosts H

    Cryptolaemus Montrouzieri As a Predator of the Striped Mealybug, Ferrisia Virgata, Reared on Two Hosts H

    J. Appl. Entomol. ORIGINAL CONTRIBUTION Cryptolaemus montrouzieri as a predator of the striped mealybug, Ferrisia virgata, reared on two hosts H. Wu1,2, Y. Zhang1, P. Liu1, J. Xie1,Y.He1, C. Deng1, P. De Clercq2 & H. Pang1 1 State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China 2 Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium Keywords Abstract biological control, cotton, Cryptolaemus montrouzieri, Ferrisia virgata, Planococcus The striped mealybug, Ferrisia virgata (Cockerell) (Hemiptera: Pseudococ- citri, prey suitability cidae), is a cosmopolitan pest of a variety of agricultural crops including cotton. To investigate the biological control potential of the predatory Correspondence ladybird Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) Hong Pang (corresponding author), State Key against this pest, we evaluated its developmental and reproductive fitness Laboratory of Biological Control, School of when feeding on F. virgata reared on pumpkin fruits or on cotton leaves Life Sciences, Sun Yat-sen University, No.135 Xingang Road West, Guangzhou 510275, and compared this to a diet of Planococcus citri Risso (Hemiptera: Pseudo- China. E-mail: [email protected] and coccidae) reared on pumpkin fruits. F. virgata and P. citri reared on pump- Patrick De Clercq (corresponding author), kins were equally suitable prey for the pre-imaginal stages of Department of Crop Protection, Faculty of C. montrouzieri. Duration of total immature development was 1 day longer Bioscience Engineering, Ghent University, in C. montrouzieri offered F. virgata reared on cotton as compared with Coupure Links 653, Ghent 9000, Belgium. F. virgata or P. citri reared on pumpkin, whereas no significant difference E-mail: [email protected] was observed in survival rates.
  • Mealybugs (Hemiptera: Pseudococcidae) Associated with Dragon Fruit in Indonesia

    Mealybugs (Hemiptera: Pseudococcidae) Associated with Dragon Fruit in Indonesia

    Advances in Biological Sciences Research, volume 8 International Conference and the 10th Congress of the Entomological Society of Indonesia (ICCESI 2019) Mealybugs (Hemiptera: Pseudococcidae) Associated with Dragon Fruit in Indonesia Dewi Sartiami 1*, Nelly Saptayanti2, Edy Syahputra3, Warastin Puji Mardiasih2, Desmawati2 1Department of Plant Protection, Faculty of Agriculture, IPB University, Bogor, West Java 16680, Indonesia 2Directorate of Horticulture Protection, Ministry of Agriculture, South Jakarta, Jakarta 12550, Indonesia 3Department of Agrotechnology, Faculty of Agriculture, University of Tanjungpura, Pontianak, West Kalimantan 78124, Indonesia *Corresponding author. Email: [email protected] ABSTRACT Mealybugs were recorded on dragon fruit, Hylocereus undatus (Family: Cactaceae) in Indonesia. The present of certain mealybug species on dragon fruit has become quarantine concern in country where the mealybugs species is absent. The objective of this study was to identify mealybugs species associated with dragon fruit and record the live specimen of adult females mealybug. Mealybugs were collected from 3 locations: Bogor (West Java), Banyuwangi (East Java), and Pontianak (West Kalimantan). Mealybugs found in the location were photographically documented and brought to the laboratory. Identification based on the prepared slide specimen was carried out in the Laboratory of Insect Biosystematics, Department of Plant Protection, Faculty of Agriculture, IPB University. There were 4 mealybugs species, Ferrisia virgata, Planococcus minor, Phenacoccus solenopsis and Pseudococcus jackbeardsleyi recorded on dragon fruit. Dragon fruit is recorded to be the new host of Ph. solenopsis. The morphological characteristics of fully developed mealy wax on live adult female were highlighted to align the characteristic diagnose of species identification based on slide mount specimen. Keywords: adult female, fruits, Hylocerus undulatus, quarantine 1.
  • Paracoccus Marginatus, an Invasive Mealybug of Papaya and Its Biological Control – an Overview M

    Paracoccus Marginatus, an Invasive Mealybug of Papaya and Its Biological Control – an Overview M

    Journal of Biological Control, 26 (3): 201–216, 2012 Review Article Paracoccus marginatus, an invasive mealybug of papaya and its biological control – An overview M. MANI, C. SHIVARAJU and A. N. SHYLESHA* Division of Entomology & Nematology Indian Institute of Horticultural Research, Hessaraghatta, Bangalore 560 089, Karnataka, India *National Bureau of Agriculturally Important Insects, Bangalore 560 024, Karnataka, India *Corresponding author: E-mail: [email protected] ABSTRACT: The papaya mealybug, Paracoccus marginatus Williams and Granara de Willink (Hemiptera: Pseudococcidae) is native of Mexico and /or Central and North America. Since its description in 1992, it has invaded several Carbbean Islands, Florida, Sri Lanka, Indonesia, Taiwan, India, Bangladesh, West Africa, and it is likely to spread many other countries. It is highly polyphagus attacking more than 70 plant species causing severe loss. Insecticides failed to give adequate control of P. marginatus. On the other hand, natural enemies particularly, Acerophagus papayae Noyes and Schauff were highly useful to suppress the papaya mealybug. Its origin, distribution, taxonomy, biology, ecology, host range, natural enemies and methods of control particularly classical biological control are reviewed here. KEY WORDS: Paracoccus marginatus, invasive mealybug, Acerophagus papayae, biology, distribution, host range, natural enemies, taxonomy, classical biological control. (Article chronicle: Received: 30-05-2012 Revised: 16-06-2012 Accepted: 18-06-2012) INTRODUCTION Dominican Republic (CABI/EPPO, 2000) and Grenada in 1994, Antigua and Barbuda (CABI/EPPO, 2000), Saint Mealybugs throughout the world cause various Martin (Pollard, 1999) and The British Virgin Islands in economic problems. Paracoccus marginatus Williams 1996 (CABI/EPPO, 2000); USA (Florida) (Pollard,1999; and Granara de Willink, popularly known as papaya Miller and Miller, 2002; Walker et al., 2006), Haiti, mealybug (PMB) has invaded several countries and St.
  • 2018 Myanmar PERSUAP

    2018 Myanmar PERSUAP

    BUREAUS FOR ASIA AND FOOD SECURITY PESTICIDE EVALUATION REPORT AND SAFE USE ACTION PLAN (PERSUAP) IEE AMENDMENT: §216.3(B) PESTICIDE PROCEDURES PROJECT/ACTIVITY DATA Project/Activity Name: Feed the Future Cambodia Harvest II (“Harvest II”) Amendment #: 1 Geographic Location: South East Asia (Cambodia) Implementation Start/End: 1/1/2017 to 12/31/2021 Implementing Partner(s): Abt Associates, International Development Enterprises (iDE), Emerging Markets Consulting (EMC) Tracking ID/link: Tracking ID/link of Related IEE: Asia 16-042 https://ecd.usaid.gov/repository/pdf/46486.pdf Tracking ID/link of Other Related Analyses: ORGANIZATIONAL/ADMINISTRATIVE DATA Implementing Operating Unit: Cambodia Funding Operating Unit: Bureau for Asia Initial Funding Account(s): $17.5 M Total Funding Amount: Amendment Funding Date / Amount: April 2017-April 2022 Other Affected Units: Bureau for Food Security Lead BEO Bureau: Asia Prepared by: Alan Schroeder, PhD, MBA; Kim Hian Seng, PhD, with support from Abt Associates and iDE Date Prepared: 8/2/2018 ENVIRONMENTAL COMPLIANCE REVIEW DATA Analysis Type: §216.3(B) Pesticide Procedures - PERSUAP Environmental Determination: Negative Determination with Conditions PERSUAP Procedures Expiration Date: 12/31/2021 Climate Risks Considerations / Conditions 2018 Feed the Future Cambodia Harvest II PERSUAP 1 ACRONYMS AI Active Ingredient A/COR Agreement/Contracting Officer’s Representative ASIA Bureau for Asia BEO Bureau Environmental Officer BMP Best Management Practice BRC British Retail Consortium BT Bacillus thuringiensis
  • Hemiptera, Pseudococcidae) on Cotton

    Hemiptera, Pseudococcidae) on Cotton

    Revista Brasileira de Entomologia http://dx.doi.org/10.1590/S0085-56262014000100012 Population growth and within-plant distribution of the striped mealybug Ferrisia virgata (Cockerell) (Hemiptera, Pseudococcidae) on cotton Martin D. Oliveira1, Christian S. A. Silva-Torres1, Jorge B. Torres1,3 & José E. Morais Oliveira2 1Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171–900 Recife-PE. [email protected], [email protected] 2Embrapa Semiárido BR 428, Km 152, Zona Rural – Caixa Postal 23, 56302–970 Petrolina-PE. [email protected] 3Corresponding author: [email protected] ABSTRACT. Population growth and within-plant distribution of the striped mealybug Ferrisia virgata (Cockerell) (Hemiptera, Pseudococcidae) on cotton. The striped mealybug, Ferrisia virgata (Cockerell) (Hemiptera, Pseudococcidae), is a widely distri- buted and polyphagous pest species, which naturally occurs on cotton plants in Brazil. This study evaluated the establishment and population growth as well as the within-plant distribution of F. virgata on four cotton cultivars: CNPA 7H (white fibers), BRS Verde, BRS Safira, and BRS Rubi (colored fibers). The experiment was conducted in a complete randomized design with four treatments (cultivars) and 18 replications of each. Thus, cotton plants of each cultivar were infested with 100 newly hatched nymphs of F. virgata. The number of adult female mealybugs and the total number of mealybugs per plant were quantified, respectively, at 25 and 50 days after infestation. The developmental and pre-reproductive periods were also determined. Further- more, we verified the distribution of F. virgata on the plant parts at 25 and 50 days after infestation.